Maternal licorice consumption during pregnancy and pubertal, cognitive, and psychiatric outcomes in children

American Journal of Epidemiology

Volumn 185, Issue 5, 2017, Pages 317-328

  Räikkönen, Katri ^a   Martikainen, Silja ^a   Pesonen, Anu Katriina ^a   Lahti, Jari ^a   Heinonen, Kati ^a   Pyhälä, Riikka ^a   Lahti, Marius ^a   Tuovinen, Soile ^a   Wehkalampi, Karoliina ^b   Sammallahti, Sara ^a   Kuula, Liisa ^a   Andersson, Sture ^b   Eriksson, Johan G ^c,d   Ortega Alonso, Alfredo ^a   Reynolds, Rebecca M ^e   Strandberg, Timo E ^c,f   Seckl, Jonathan R ^e   Kajantie, Eero ^g,h  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI AND HELSINKI UNIVERSITY HOSPITAL   (Finland)

^c HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^d FOLKHÄLSAN RESEARCH CENTER   (Finland)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

^f UNIVERSITY OF OULU   (Finland)

^g NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^h OULU UNIVERSITY HOSPITAL   (Finland)

Author keywords

11 hydroxysteroid dehydrogenase type 2; ADHD; Cognition; Glucocorticoids; Glycyrrhizin; Puberty

Indexed keywords

DEXAMETHASONE; GLYCYRRHIZIC ACID; HYDROCORTISONE; ANTIINFLAMMATORY AGENT;

BODY MASS; CHILD HEALTH; CONFIDENCE INTERVAL; HEALTH RISK; HERB; INHIBITION; MATERNAL HEALTH; MENTAL HEALTH; PREGNANCY; PSYCHOLOGY; STEROID;

ADULT; ARTICLE; ASSESSMENT OF HUMANS; ATTENTION; ATTENTION DEFICIT DISORDER; BODY HEIGHT; BODY MASS; BODY WEIGHT; CHILD; CHILD BEHAVIOR CHECKLIST; COGNITION; COHORT ANALYSIS; COMPARATIVE STUDY; CONTINUOUS PERFORMANCE TEST; EXECUTIVE FUNCTION; FEMALE; GLYCYRRHIZA; HUMAN; INTELLIGENCE QUOTIENT; LONGITUDINAL STUDY; LOW DRUG DOSE; MALE; MEMORY; MENTAL DISEASE; NEUROENDOCRINE SYSTEM; NEUROPSYCHOLOGICAL TEST; NEUROTOXICITY; PERCEPTION; PREGNANCY; PREGNANT WOMAN; PRENATAL EXPOSURE; PROGENY; PUBERTAL DEVELOPMENT SCALE; PUBERTY; SALIVA LEVEL; SCHOOL CHILD; SOCIAL LEARNING; TRAIL MAKING TEST; WISCONSIN CARD SORTING TEST; ADOLESCENT; ADVERSE EFFECTS; CHEMICALLY INDUCED; CHEMISTRY; DRUG EFFECTS; EPIDEMIOLOGY; FINLAND; FOLLOW UP; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; INTELLIGENCE; SALIVA; SEX RATIO; SEXUAL MATURATION;

FINLAND; HELSINKI; VARSINAIS-SUOMI;

ANIMALIA; GLYCYRRHIZA;

ADOLESCENT; ANTI-INFLAMMATORY AGENTS; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; BODY MASS INDEX; CHILD; CONFOUNDING FACTORS (EPIDEMIOLOGY); DEXAMETHASONE; FEMALE; FINLAND; FOLLOW-UP STUDIES; GLYCYRRHIZA; GLYCYRRHIZIC ACID; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INTELLIGENCE; MALE; PITUITARY-ADRENAL SYSTEM; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SALIVA; SEX DISTRIBUTION; SEXUAL MATURATION;

EID: 85019740011     PISSN: 00029262     EISSN: 14766256     Source Type: Journal    
DOI: 10.1093/aje/kww172     Document Type: Article

References (42)

1. World Cancer Research Fund; American Institute for Cancer Research. Food Nutrition, Physical Activity, and the Prevention of Cancer: A Global Perspective. Washington, DC: American Institute for Cancer Research; 2007.
2. Prentice P, Viner RM. Pubertal timing and adult obesity and cardiometabolic risk in women and men: a systematic review and meta-analysis. Int J Obes (Lond). 2013;37(8):1036-1043.
3. Joinson C, Heron J, Araya R, et al. Association between pubertal development and depressive symptoms in girls from a UK cohort. Psychol Med. 2012;42(12):2579-2589.
4. Barker DJ. Developmental origins of adult health and disease. J Epidemiol Community Health. 2004;58(2): 114-115.
5. Räikkönen K, Forsén T, Henriksson M, et al. Growth trajectories and intellectual abilities in young adulthood: the Helsinki Birth Cohort study. Am J Epidemiol. 2009;170(4): 447-455.
6. Gitau R, Cameron A, Fisk NM, et al. Fetal exposure to maternal cortisol. Lancet. 1998;352(9129):707-708.
7. Seckl JR, Meaney MJ. Glucocorticoid programming. Ann NY Acad Sci. 2004;1032:63-84.
8. Edwards CR, Benediktsson R, Lindsay RS, et al. Dysfunction of placental glucocorticoid barrier: link between fetal environment and adult hypertension? Lancet. 1993; 341(8841):355-357.
9. Benediktsson R, Calder AA, Edwards CR, et al. Placental 11 beta-hydroxysteroid dehydrogenase: a key regulator of fetal glucocorticoid exposure. Clin Endocrinol (Oxf). 1997;46(2): 161-166.
10. Holmes MC, Abrahamsen CT, French KL, et al. The mother or the fetus? 11β-hydroxysteroid dehydrogenase type 2 null mice provide evidence for direct fetal programming of behavior by endogenous glucocorticoids. J Neurosci. 2006; 26(14):3840-3844.
11. Welberg LA, Seckl JR, Holmes MC. Inhibition of 11β-hydroxysteroid dehydrogenase, the foeto-placental barrier to maternal glucocorticoids, permanently programs amygdala GR mRNA expression and anxiety-like behavior in the offspring. Eur J Neurosci. 2000;12(3):1047-1054.
12. Wyrwoll CS, Holmes MC. Prenatal excess glucocorticoid exposure and adult affective disorders: a role for serotonergic and catecholamine pathways. Neuroendocrinology. 2012; 95(1):47-55.
13. Zambrano E, Guzmán C, Rodríquez-González GL, et al. Fetal programming of sexual development and reproductive function. Mol Cell Endocrinol. 2014;382(1):538-549.
14. Brown RW, Diaz R, Robson AC, et al. The ontogeny of 11 beta-hydroxysteroid dehydrogenase type 2 and mineralocorticoid receptor gene expression reveal intricate control of glucocorticoid action in development. Endocrinology. 1996;137(2):794-797.
15. Teelucksingh S, Benediktsson R, Lindsay RS, et al. Liquorice. Lancet. 1991;337(8756):1549.
16. Strandberg TE, Järvenpää AL, Vanhanen H, et al. Birth outcome in relation to licorice consumption during pregnancy. Am J Epidemiol. 2001;153(11):1085-1088.
17. Räikkönen K, Pesonen AK, Heinonen K, et al. Maternal licorice consumption and detrimental cognitive and psychiatric outcomes in children. Am J Epidemiol. 2009: 170(9):1137-1146.
18. Räikkönen K, Seckl JR, Heinonen K, et al. Maternal prenatal licorice consumption alters hypothalamic-pituitary-adrenocortical axis function in children. Psychoneuroendocrinology. 2010; 35(10):1587-1593.
19. Robins JM, Rotnitzky A, Zhao LP. Analysis of semiparametric regression models for repeated outcomes in the presence of missing data. J Am Stat Assoc. 1995;90(429):106-121.
20. Austin PC, Stuart EA. Moving towards best practice when using inverse probability of treatment weighting (IPTW) using the propensity score to estimate causal treatment effects in observational studies. Stat Med. 2015;34(28):3661-3679.
21. Saari A, Sankilampi U, Hannila ML, et al. New Finnish growth references for children and adolescents aged 0 to 20 years: length/height-for age, weight-for-length/height, and body mass index-for-age. Ann Med. 2011;43(3):235-248.
22. Sorva R, Tolppanen EM, Lankinen S, et al. Growth evaluation: parent and child specific height standards. Arch Dis Child. 1989;64(10):1483-1487.
23. Morris NM, Udry JR. Validation of a self-administered instrument to assess stage of adolescent development. J Youth Adolesc. 1980;9(3):271-280.
24. Petersen AC, Crockett L, Richards M, et al. A self-report measure of pubertal status: reliability, validity, and initial norms. J Youth Adolesc. 1980;17(2):117-133.
25. Wechsler D. WISC-III: Wechsler Intelligence Scale for Children: Manual. 3rd ed. San Antonio, TX: The Psychological Corporation; 1991.
26. Kaufman AS, Kaufman JC, Ramaswamy B, et al. Comparison of three WISC-III short forms: weighing psychometric, clinical, and practical factors. J Clin Child Psychol. 1996;25(1):97-105.
27. Korkman M, Kirk U, Kemp S. NEPSY-II: Clinical and Interpretative Manual. 2nd ed. San Antonio, TX: Harcourt Assessment; 2007.
28. Conners CK. Conners' Continuous Performance Test (CPT II). Toronto, ON, Canada: Multi Health Systems; 2004.
29. Lezak MD. Neuropsychological Assessment. 4th ed. New York, NY: Oxford University Press; 2004.
30. Heaton RK. WCST-64: Computer Version for Windows-Research edition. Odessa, FL: Psychological Assessment Resources; 2000.
31. Achenbach TM, Rescorla LA. Manual for the ASEBA School-Age Forms and Profiles. Burlington, VT: University of Vermont, Research Center for Children, Youth, and Families; 2001.
32. Martikainen S, Pesonen A-K, Lahti J, et al. Physical activity and hypothalamic-pituitary-adrenal axis function in adolescents. Psychoneuroendocrinology. 2014;49:96-105.
33. Wehkalampi K, Hovi P, Dunkel L, et al. Advanced pubertal growth spurt in subjects born preterm: the Helsinki Study of Very Low Birth Weight Adults. J Clin Endocrinol Metab. 2011;96(2):525-533.
34. Bijlsma J, Van Vloten P, Van Gelderen C, et al. An Assessment of the Effects of Various Dosages of Glycyrrhizin in Healthy Female Volunteers [in Dutch]. Bilthoven, The Netherlands: RIVM; 1996 (RIVM report no. 348801004).
35. US Food and Drug Administration. Listing of specific substances affirmed as generally recognized as safe. United States Food and Drug Administration: licorice and licorice derivatives. Code of Federal Regulations, 21CFR184.1408. (April 1, 2016).
36. Rasmussen A, Wohlfahrt-Veje C, Tefre de Renzy-Martin K, et al. Validity of self-assessment of pubertal maturation. Pediatrics. 2015;135(1):86-93.
37. Coleman L, Coleman J. The measurement of puberty: a review. J Adolesc. 2002;25(5):535-550.
38. Isbrucker RA, Burdock GA. Risk and safety assessment on the consumption of licorice root (Glycyrrhiza sp.), its extract, powder as a food ingredient with emphasis on the pharmacology and toxicology of glycyrrhizin. Regul Toxicol Pharmacol. 2006; 46(3):167-192.
39. Flak AL, Su S, Bertrand J, et al. The association of mild, moderate, and binge prenatal alcohol exposure and child neuropsychological outcomes: a meta-analysis. Alcohol Clin Exp Res. 2014;38(1):214-226.
40. World Health Organization. Global Status Report on Alcohol and Health 2014. Geneva, Switzerland: World Health Organization; 2014.
41. European Commission. Opinion of the Scientific Committee on Food on Glycyrrhizinic Acid and Its Ammonium Salt. (European Commission Scientific Committee on Food report SCF/CS/ADD/EDUL/255, Final, April 10, 2003). Brussels, Belgium: European Commission; 2003.
42. World Health Organization. Evaluation of Certain Food Additives: Sixty-Third Report of the Joint FAO/WHO Expert Committee on Food Additives. Geneva, Switzerland: World Health Organization; 2005. (WHO Technical Report Series no. 928).